Current Status, Problems and Prospects of Entomopathogenic Fungi in Controlling Fall Armyworm Spodoptera frugiperda

doi:10.16409/j.cnki.2095-039x.2019.05.030

Abstract

Abstract: The fall armyworm Spodoptera frugiperda (J. E. Smith) is an important agricultural pest worldwide, damages crops seriously and is difficult to control. Entomopathogenic fungi have abundant strains with some important advantages in controlling insect pests, e.g. easy prevalence, hardly eliciting resistance in insect pests. Thus, they have great potential in controlling the fall armyworm. To make full use of entomopathogenic fungi in S. frugiperda control, we reviewed here the current status and analyze problems existing in control of the fall armyworm with fungal pathogen. Directions in future research on controlling of S. frugiperda with entomopathogenic fungi were also proposed.

Key words: Spodoptera frugiperda, chemical pesticide, resistance, fungal pesticide, integrated pest management

CLC Number:

S476.1

ZHANG Wei, PENG Guoxiong, XIA Yuxian. Current Status, Problems and Prospects of Entomopathogenic Fungi in Controlling Fall Armyworm Spodoptera frugiperda[J]. Chinese Journal Of Biological Control, 2019, 35(5): 674-681.

References

[1] 喜超, 姜玉英, 木霖, 等. 草地贪夜蛾在云南的潜在适生区分析及经济损失预测[J]. 南方农业学报, 2019, 50(6):1226-1233.
[2] Hruska A J, Gould F. Fall armyworm (Lepidoptera:Noctuidae) and Diatraea lineolata (Lepidoptera:Pyralidae):Impact of larval population level and temporal occurrence on maize yield in Nicaragua[J]. Journal of Economic Entomology, 1997, 90(2):611-622.
[3] Prasanna B M, Huesing J E, Eddy R, et al. Fall armyworm in Africa:a guide for integrated pest management[R]. Mexico, CDMX:CIMMYT, 2018.
[4] 郭井菲, 何康来, 王振营. 草地贪夜蛾的生物学特性, 发展趋势及防控对策[J]. 应用昆虫学报, 2019, 56(3):361-369.
[5] 李红梅, 万敏, 顾蕊, 等. 基于文献计量学的重大入侵害虫草地贪夜蛾的研究动态分析[J]. 植物保护, 2019, 45(4):34-42.
[6] 李永平, 张帅, 王晓军, 等. 草地贪夜蛾抗药性现状及化学防治策略[J]. 植物保护, 2019, 45(4):14-19.
[7] 王芹芹, 崔丽, 王立, 等. 草地贪夜蛾对杀虫剂的抗性研究进展[J]. 农药学学报, 2019, 21(4):401-408.
[8] 吴超, 张磊, 廖重宇, 等. 草地贪夜蛾对化学农药和Bt作物的抗性机制及其治理技术研究进展[J]. 植物保护学报, 2019, 46(3):503-513.
[9] 陈万斌, 李玉艳, 王孟卿, 等. 草地贪夜蛾的昆虫病原微生物资源及其应用现状[J]. 植物保护, 2019, DOI:10.16688/j.zwbh.2019453.
[10] 陈万斌, 王孟卿, 刘晨曦, 等. 草地贪夜蛾的天敌昆虫资源、应用现状及存在的问题与建议[J]. 中国生物防治学报, 2019, DOI:10.16409/j.cnki.2095-039x.2019.05.013.
[11] Shylesha A N, Jalali S K, Gupta A, et al. Studies on new invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera:Noctuidae) and its natural enemies[J]. Journal of Biological Control, 2018, 32(3):1-7.
[12] Akutse K S, Kimemia J W, Ekesi S, et al. Ovicidal effects of entomopathogenic fungal isolates on the invasive fall armyworm Spodoptera frugiperda (Lepidoptera:Noctuidae)[J]. Journal of Applied Entomology, 2019, 143(6):626-634.
[13] García C, Bautista N. Pathogenicity of isolates of entomopathogenic fungi against Spodoptera frugiperda (Lepidoptera:Noctuidae) and Epilachna varivestis (Coleoptera:Coccinellidae)[J]. Revista Colombiana de Entomología, 2011, 37(2):217-222.
[14] Carneiro A A, Gomes E A, Guimarães C T, et al. Molecular characterization and pathogenicity of isolates of Beauveria spp. to fall armyworm[J]. Pesquisa Agropecuária Brasileira, 2008, 43(4):513-520.
[15] Thomazoni D, Formentini M A, Alves L F A. Patogenicidade de isolados de fungos entomopatogênicos à Spodoptera frugiperda (Smith) (Lepidoptera:Noctuidae)[J]. Arquivos do Instituto Biológico, 2014, 81(2):126-133.
[16] 郑亚强, 胡惠芬, 付玉飞, 等. 草地贪夜蛾莱氏绿僵菌的分离鉴定[J]. 植物保护, 2019, DOI:10.16688/j.zwbh.2019399.
[17] 程东美, 洪婉雯, 孙辉, 等. 草地贪夜蛾幼虫僵虫发生率调查及致病菌分离鉴定[J]. 环境昆虫学报, http://kns.cnki.net/kcms/detail/44,1640.Q.20190717.1722.002.html, (2019-09-13).
[18] 赵胜园, 杨现明, 孙小旭, 等. 常用生物农药对草地贪夜蛾的室内防效[J]. 植物保护, 2019, 45(3):21-26.
[19] Srivastava C N, Maurya P, Sharma P, et al. Prospective role of insecticides of fungal origin[J]. Entomological Research, 2009, 39(6):341-355.
[20] 谭清, 高熹, 庞仁乙, 等. 家蝇不同虫态附着蜡蚧轮枝菌分生孢子能力及与其体表结构的关系[J]. 南方农业学报, 2015, 46(2):241-249.
[21] Siebert M W, Tindall K V, Leonard B R, et al. Evaluation of corn hybrids expressing CrylF (Herculex^® I insect protection) against fall armyworm (Lepidoptera:Noctuidae) in the southern United States[J]. Journal of Entomological Science, 2008, 43(1):41-51.
[22] Pannuti L E R, Baldin E L L, Hunt T E, et al. On-plant larval movement and feeding behavior of fall armyworm (Lepidoptera:Noctuidae) on reproductive corn stages[J]. Environmental Entomology, 2015, 45(1):192-200.
[23] 徐玲, 张鸭关, 陈自宏, 等. 4种虫生真菌对储粮害虫黄粉虫不同虫态的生防研究[J]. 西南农业学报, 2017, 30(8):1784-1789.
[24] Ekesi S, Maniania N K. Susceptibility of Megalurothrips sjostedti developmental stages to Metarhizium anisopliae and the effects of infection on feeding, adult fecundity, egg fertility and longevity[J]. Entomologia Experimentalis et Applicata, 2000, 94(3):229-236.
[25] 闫鹏飞, 孙跃先, 邓裕亮, 等. 蜡蚧轮枝菌KMZW-1菌株对扶桑绵粉蚧的毒力测定[J]. 华中农业大学学报, 2013, 32(4):38-42.
[26] Leger R J S T, Joshi L, Bidochka M J, et al. Construction of an improved mycoinsecticide overexpressing a toxic protease[J]. Proceedings of the National Academy of Sciences, 1996, 93(13):6349-6354.
[27] Fang W, Leng B, Xiao Y, et al. Cloning of Beauveria bassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence[J]. Applied and Environmental Microbiology, 2005, 71(1):363-370.
[28] Peng G, Xia Y. Integration of an insecticidal scorpion toxin (Bjα IT) gene into Metarhizium acridum enhances fungal virulence towards Locusta migratoria manilensis[J]. Pest Management Science, 2015, 71(1):58-64.
[29] Hu J, Xia Y. Increased virulence in the locust-specific fungal pathogen Metarhizium acridum expressing dsRNAs targeting the host F1F0-ATPase subunit genes[J]. Pest Management Science, 2019, 75(1):180-186.
[30] Zhang S, Xia Y X, Kim B, et al. Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana[J]. Molecular Microbiology, 2011, 80(3):811-826.
[31] Li J, Ying S H, Shan L T, et al. A new non-hydrophobic cell wall protein (CWP10) of Metarhizium anisopliae enhances conidial hydrophobicity when expressed in Beauveria bassiana[J]. Applied Microbiology and Biotechnology, 2010, 85(4):975-984.
[32] Ortiz-Urquiza A, Keyhani N. Action on the surface:entomopathogenic fungi versus the insect cuticle[J]. Insects, 2013, 4(3):357-374.
[33] Wang C, Leger R J S. The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence[J]. Journal of Biological Chemistry, 2007, 282(29):21110-21115.
[34] Wang S, Fang W, Wang C, et al. Insertion of an esterase gene into a specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars[J]. PLoS Pathogens, 2011, 7(6):e1002097.
[35] Zhang W, Chen J, Keyhani N O, et al. Comparative transcriptomic analysis of immune responses of the migratory locust, Locusta migratoria, to challenge by the fungal insect pathogen, Metarhizium acridum[J]. BMC Genomics, 2015, 16(1):867.
[36] Yang Z, Jiang H, Zhao X, et al. Correlation of cell surface proteins of distinct Beauveria bassiana cell types and adaption to varied environment and interaction with the host insect[J]. Fungal Genetics and Biology, 2017, 99:13-25.
[37] Wang C, Leger R J S. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses[J]. Proceedings of the National Academy of Sciences, 2006, 103(17):6647-6652.
[38] Wang B, Kang Q, Lu Y, et al. Unveiling the biosynthetic puzzle of destruxins in Metarhizium species[J]. Proceedings of the National Academy of Sciences, 2012, 109(4):1287-1292.
[39] Feng P, Shang Y, Cen K, et al. Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity[J]. Proceedings of the National Academy of Sciences, 2015, 112(36):11365-11370.
[40] Fan Y, Liu X, Keyhani N O, et al. Regulatory cascade and biological activity of Beauveria bassiana oosporein that limits bacterial growth after host death[J]. Proceedings of the National Academy of Sciences, 2017, 114(9):E1578-E1586.
[41] 陈春, 冯明光. 桃蚜迁飞性有翅蚜携带传播蚜虫病原真菌的证据[J]. 科学通报, 2002, 47(17):1332-1334.
[42] 黄志宏. 云南低纬度高原地区随寄主迁飞扩散传播的蚜虫病原真菌以及努利虫疠霉的侵染生物学特征[D]. 杭州:浙江大学, 2008.
[43] 彭凡, 黄勃, 周根土, 等. 虫生真菌在准格尔旗沙棘木蠹蛾上的流行[J]. 经济林研究, 2007(4):38-40, 49.
[44] 董辉, 苏红田, 高松, 等. 绿僵菌对蝗虫及其捕食性天敌的影响[J]. 中国生物防治, 2005, 21(1):60-62.
[45] Flexner J L, Lighthart B, Croft B A. The effects of microbial pesticides on non-target, beneficial arthropods[J]. Agriculture, Ecosystems & Environment, 1986, 16(3-4):203-254.
[46] 唐艺婷, 李玉艳, 刘晨曦, 等. 蠋蝽对草地贪夜蛾的捕食能力评价和捕食行为观察[J]. 植物保护, 2019, 45(4):65-68.
[47] 唐艺婷, 王孟卿, 陈红印, 等. 益蝽对草地贪夜蛾的捕食能力评价和捕食行为观察[J]. 中国生物防治学报, 2019, DOI:10.16409/j.cnki.2095-039x. 2019.04.005.
[48] 徐庆宣, 王松, 田仁斌, 等. 大草蛉对草地贪夜蛾捕食潜能研究[J]. 环境昆虫学报, 2019, 41(4):754-759.
[49] 赵雪晴, 刘莹, 石旺鹏, 等. 东亚小花蝽对草地贪夜蛾幼虫的捕食效应[J]. 植物保护, 2019, DOI:10.16688/j.zwbh.2019375.
[50] 代晓彦, 翟一凡, 陈福寿, 等. 东亚小花蝽对草地贪夜蛾幼虫的捕食能力评价[J]. 中国生物防治学报, 2019, DOI:10.16409/j.cnki.2095-039x. 2019.05.003.
[51] 赵英杰, 郑亚强, 符成悦, 等. 异色瓢虫对草地贪夜蛾2龄幼虫的捕食功能反应[J]. 植物保护, 2019, DOI:10.16688/j.zwbh.2019370.
[52] 刘本菊, 秦得强, 周游, 等. 异色瓢虫对草地贪夜蛾的捕食行为观察与评价[J]. 华南农业大学学报, http://kns.cnki.net/kcms/detail/44.1110.S.20190828.2122.002.html, (2019-09-13)
[53] 李志刚, 吕欣, 押玉柯, 等. 粤港两地田间发现夜蛾黑卵蜂与螟黄赤眼蜂寄生草地贪夜蛾[J]. 环境昆虫学报, 2019, 41(4):760-765.
[54] 陈壮美, 赵琳超, 刘航, 等. 斯氏侧沟茧蜂对草地贪夜蛾幼虫的寄生行为及寄生效应[J]. 植物保护, 2019, DOI:10.16688/j.zwbh.2019341.
[55] 戴鹏, 孙佳伟, 陈永明, 等. 赞比亚发现三种防治草地贪夜蛾的卵寄生蜂简报[J]. 吉林农业大学学报, 2019, DOI:10.13327/j.jjlau.2019.5310.
[56] Hong M, Peng G, Keyhani N O, et al. Application of the entomogenous fungus, Metarhizium anisopliae, for leafroller (Cnaphalocrocis medinalis) control and its effect on rice phyllosphere microbial diversity[J]. Applied Microbiology and Biotechnology, 2017, 101(17):6793-6807.
[57] Vega F E. The use of fungal entomopathogens as endophytes in biological control:a review[J]. Mycologia, 2018, 110(1):4-30.
[58] Behie S W, Jones S J, Bidochka M J. Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria[J]. Fungal Ecology, 2015, 13:112-119.
[59] Mantzoukas S, Chondrogiannis C, Grammatikopoulos G. Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer S esamia nonagrioides[J]. Entomologia Experimentalis et Applicata, 2015, 154(1):78-87.
[60] Batta Y A. Efficacy of endophytic and applied Metarhizium anisopliae (Metch.) Sorokin (Ascomycota:Hypocreales) against larvae of Plutella xylostella L. (Yponomeutidae:Lepidoptera) infesting Brassica napus plants[J]. Crop Protection, 2013, 44(1):128-134.
[61] Ramirez-Rodriguez D, Sánchez-Peña S R. Endophytic Beauveria bassiana in Zea mays:Pathogenicity against Larvae of Fall Armyworm, Spodoptera frugiperda[J]. Southwestern Entomologist, 2016, 41(3):875-879.
[62] 樊学珍, 李增智. 绿僵菌在土壤中的延续及控制桃小食心虫的潜力[J]. 应用生态学报, 1996, 7(1):49-55.
[63] Granzow S, Kaiser K, Wemheuer B, et al. The effects of cropping regimes on fungal and bacterial communities of wheat and faba bean in a greenhouse pot experiment differ between plant species and compartment[J]. Frontiers in Microbiology, 2017, 8:902.
[64] Yaroslavtseva O N, Dubovskiy I M, Khodyrev V P, et al. Immunological mechanisms of synergy between fungus Metarhizium robertsii and bacteria Bacillus thuringiensis ssp. morrisoni on Colorado potato beetle larvae[J]. Journal of Insect Physiology, 2017, 96(1):14-20.
[65] 王卅. 八角茴香提取物与几种绿僵菌对桃蚜的协同作用研究[D]. 合肥:安徽农业大学, 2016.
[66] 夏成润, 丁德贵, 刘云鹏, 等. 金龟子绿僵菌无纺布菌剂与引诱剂结合使用防治短角幽天牛的试验[J]. 安徽农业大学学报, 2005, 32(4):15-18.
[67] 秦兴虎, 吴惠惠, 王广君, 等. 以绿步甲为载体携播绿僵菌对东亚飞蝗的协同控制作用研究[J]. 中国生物防治学报, 2015, 31(2):284-290.
[68] Yu S J, Nguyen S N, Abo-Elghar G E. Biochemical characteristics of insecticide resistance in the fall armyworm, Spodoptera frugiperda (J. E. Smith)[J]. Pesticide Biochemistry and Physiology, 2003, 77(1):1-11.
[69] Carvalho R A, Omoto C, Field L M, et al. Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the fall armyworm Spodoptera frugiperda[J]. PLoS ONE, 2013, 8(4):e62268.
[70] Boaventura D, Bolzan A, Padovez F E O, et al. Detection of a ryanodine receptor target-site mutation in diamide insecticide resistant fall armyworm, Spodoptera frugiperda[J]. Pest Management Science, 2019, DOI:10.1002/ps.5505.
[71] Nascimento A R B, FariaS J R, Bernardi D, et al. Genetic basis of Spodoptera frugiperda (Lepidoptera:Noctuidae) resistance to the chitin synthesis inhibitor lufenuron[J]. Pest Management Science, 2016, 72(4):810-815.
[72] Rivero-Borja M, Guzmán-Franco A W, Rodríguez-Leyva E, et al. Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae[J]. Pest Management Science, 2018, 74(9):2047-2052.
[73] Farenhorst M, Mouatcho J C, Kikankie C K, et al. Fungal infection counters insecticide resistance in African malaria mosquitoes[J]. Proceedings of the National Academy of Sciences, 2009, 106(41):17443-17447.
[74] McGaughey W H, Whalon M E. Managing insect resistance to Bacillus thuringiensis toxins[J]. Science, 1992, 258(5087):1451-1455.
[75] Farias J R, Andow D A, Horikoshi R J, et al. Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera:Noctuidae) in Brazil[J]. Crop Protection, 2014, 64(1):150-158.
[76] Omoto C, Bernardi O, Salmeron E, et al. Field-evolved resistance to Cry1Ab maize by Spodoptera frugiperda in Brazil[J]. Pest Management Science, 2016, 72(9):1727-1736.
[77] Bernardi O, Bernardi D, Ribeiro R S, et al. Frequency of resistance to Vip3Aa20 toxin from Bacillus thuringiensis in Spodoptera frugiperda (Lepidoptera:Noctuidae) populations in Brazil[J]. Crop Protection, 2015, 76(1):7-14.
[78] Storer N P, Babcock J M, Schlenz M, et al. Discovery and characterization of field resistance to Bt maize:Spodoptera frugiperda (Lepidoptera:Noctuidae) in Puerto Rico[J]. Journal of Economic Entomology, 2010, 103(4):1031-1038.
[79] Huang F, Qureshi J A, Meagher JR R L, et al. Cry1F resistance in fall armyworm Spodoptera frugiperda:single gene versus pyramided Bt maize[J]. PLoS ONE, 2014, 9(11):e112958.